The Extended Phenotype: The Long Reach of the Gene (Popular Science) (29 page)

I suppose ‘outnumbering’ could, in practice, work in two main ways. Firstly, if different modifiers each cause a quantitative diminution of the outlaw’s effect, several modifiers might combine additively. Secondly, if any one of several modifiers would suffice to neutralize the outlaw, the chance of effective neutralization goes up with the number of available modifier loci. Alexander and Borgia’s metaphor of ‘outnumbering’, and Leigh’s metaphor of the power of the collective in a ‘parliament’ of the many, could be given meaning in either or both of these two ways. It is important for the argument that segregation distorters at different loci could not, in any obvious sense, ‘pool their efforts’. They are not working for some common end of ‘general segregation distortion’. Rather, each one is working to distort segregation in favour of itself, and this will hurt other segregation distorters just as much as it hurts non-distorters. Suppressors of segregation distorters, on the other hand, could, in a sense, pool their efforts.

The parliament of genes is one of those metaphors which, if we are not careful, tricks us into thinking that it explains more than it does. Like all humans, but unlike genes, human Members of Parliament are highly sophisticated computers capable of using foresight and language to conspire and reach agreements. Outlaws may seem to be suppressed by agreement of a collective in the parliament of genes, but what is really going on is the selection of modifier genes in preference to non-modifying alleles at their respective loci. Needless to say, Leigh and the other advocates of the ‘parliament of genes’ hypothesis are well aware of this. I now want to extend the list of outlaws.

If a segregation distorter occurs on a sex chromosome, it is not only an outlaw in conflict with the rest of the genome and therefore subject to suppression by modifiers: it also, incidentally, threatens the whole population with extinction. This is because, in addition to ordinary detrimental side effects, it also distorts the sex ratio, and may even eliminate one sex from the population altogether. In one of Hamilton’s (1967) computer simulations, a single mutant male with a ‘driving Y’ chromosome causing males to have only sons and no daughters, was introduced into a population of 1000 males and 1000 females. It took only fifteen generations to drive the model population extinct for lack of females. Something like this effect has been demonstrated in the laboratory (Lyttle 1977). The possibility of using a driving Y gene in the control of serious pests like the yellow-fever mosquito did not escape Hickey and Craig (1966). It is a method with sinister elegance because it is so cheap: all the work of spreading the pest control agent is done by the pests themselves together with natural selection. It is like ‘germ warfare’ except that the lethal ‘germ’ is not an extraneous virus but a gene in the species’s own gene-pool. Perhaps the distinction is not a fundamental one anyway (
Chapter 9
).

X-linked drive is likely to have the same sort of detrimental effect on populations as Y-linked drive, but tends to take more generations to extinguish the population (Hamilton 1967). The driving gene on an X chromosome causes males to have daughters rather than sons (except in birds, Lepidoptera, etc.). As we saw in
Chapter 4
, if haploid male Hymenoptera could influence the amount of care devoted to their spouses’ offspring, they would favour daughters rather than sons, since males pass no genes on to sons. The mathematics of this situation are analogous to the case of X-linked drive, the whole genome of the male hymenopteran functioning like an X chromosome (Hamilton 1967, p. 481 and footnote 18).

It is often the case that X chromosomes cross over with each other but not with Y chromosomes. It follows that all genes on X chromosomes could stand to gain from the presence in the gene-pool of a driving X gene which distorts
gametogenesis in the heterogametic sex in favour of X gametes and against Y gametes. Genes on X chromosomes are, in a sense, united against Y genes, in a kind of ‘anti linkage group’, simply because they have no chance of finding themselves on a Y chromosome. Modifiers to suppress X-linked meiotic drive in the heterogametic sex might well not be favoured if they arose at other loci on X chromosomes. They would be favoured if they arose on autosomes. This is different from the case of segregation distorters on autosomes: here there might well be selection in favour of suppressing them by modifiers at other loci even on the same chromosome. X-linked distorters affecting gamete production in the heterogametic sex are, then, outlaws from the point of view of the autosomal part of the gene-pool, but not from the point of view of the rest of the X-chromosomal part of the gene-pool. This potential ‘solidarity’ among the genes on sex chromosomes suggests that the concept of the outlaw gene may be too simple. It conveys the image of a single rebel standing out against the rest of the genome. At times we might, instead, do better to think in terms of wars between rival gangs of genes, for instance the X-chromosome genes against the rest. Cosmides and Tooby (1981) coin the useful term ‘coreplicon’ for such a gang of genes that replicate together and therefore tend to work for the same ends. In many cases neighbouring coreplicons will blur into each other.

Ganging up by Y-chromosome genes is even more to be expected. As long as Y chromosomes do not cross over, it is clear that all genes on a Y chromosome stand to gain from the presence of a Y-linked distorter every bit as much as the distorter gene itself. Hamilton (1967) made the interesting suggestion that the reason for the well-known inertness of Y chromosomes (hairy ears seems to be the only conspicuous Y-linked trait in man) is that Y-suppressing modifiers have been positively selected elsewhere in the genome. It is not obvious how a modifier might go about suppressing the phenotypic activity of an entire chromosome, since the various phenotypic effects of a single chromosome are usually so heterogeneous. (Why would selection not suppress only the effects of the driving genes, leaving other Y-linked effects intact?) I suppose it might do it by physically deleting large chunks of Y chromosome, or by contriving to quarantine the Y chromosome from the cell’s transcription machinery.

A weird example of a driving replicator which is probably not a gene in the ordinary sense of the word is given by Werren, Skinner and Charnov (1981). They studied the parasitoid wasp
Nasonia vitripennis
, in which there is a variety of males called Dl, or ‘daughterless’. Wasps being haplodiploid, males pass their genes only to daughters: a male’s mate may have sons, but those sons are haploid and fatherless. When Dl males mate with females, they cause them to produce all male broods. Most of the sons of females mated to Dl males are themselves Dl males. Although no nuclear genes pass from father to son, therefore, the Dl factor somehow does pass
from father to ‘son’. The Dl factor rapidly spreads, in exactly the same way as a driving Y chromosome would. It is not known what the Dl factor physically consists of. It is certainly not nuclear genetic material, and it is theoretically possible that it is not even composed of nucleic acid, although Werren
et al
. suspect that it probably is cytoplasmically borne nucleic acid. Theoretically,
any
kind of physical or chemical influence of a Dl male on his mate, which causes her to have Dl sons, would spread like a driving Y chromosome, and would qualify as an active germ-line replicator in the sense of
Chapter 5
. It is also an outlaw
par excellence
, for it spreads itself at the total expense of all the nuclear genes in the males that bear it.

With some exceptions, all the diploid cells of an organism are genetically identical, but the haploid gametes it produces are all different. Only one out of many sperms in an ejaculate can fertilize an egg, and there is therefore potential for competition among them. Any gene that found phenotypic expression when in the haploid state in a sperm cell could be favoured over its alleles if it improved the competitive ability of the sperm. Such a gene would not necessarily be sex-linked: it could be found on any chromosome. If it was sex-linked it would have the effect of biasing the sex ratio, and would be an outlaw. If it was on an autosome it would still qualify as an outlaw for the general kind of reason already given for any segregation distorter: ‘… if there were genes affecting sperm-cell function there would be competition among sperm cells, and a gene that improved the ability to fertilize would increase in the population. If such a gene happened to cause, say, malfunction of the liver, that would be just too bad; the gene would increase anyway, since selection for good health is much less effective than selection by competition among sperm cells’ (Crow 1979). There is, of course, no particular reason why a sperm competition gene should happen to cause malfunction of the liver but, as already pointed out, most mutations are deleterious, so some undesirable side effect is pretty likely.

Why does Crow assert that selection for good health is much less effective than selection by competition among sperm cells? There must inevitably be a quantitative trade-off involving the magnitude of the effect on health. But, that aside, and even allowing for the controversial possibility that only a minority of sperms are viable (Cohen 1977), the argument appears to have force because the competition between sperm cells in an ejaculate would seem to be so fierce.

A million million spermatozoa,

All of them alive:

Out of their cataclysm but one poor Noah

Dare hope to survive.

And of that billion minus one

Might have chanced to be

Shakespeare, another Newton, a new Donne—

But the One was Me.

Shame to have ousted your betters thus.

Taking ark while the others remained outside!

Better for all of us, froward Homunculus,

If you’d quietly died!

Aldous Huxley

One might imagine that a mutant gene that expressed itself when in the haploid genotype of a spermatozoon, causing increased competitive ability, say an improved swimming tail or the secretion of a spermicide to which the sperm itself was immune, would be immediately favoured by a selection pressure gigantic enough to outweigh all but the most catastrophic of deleterious side effects on the diploid body. But although it may be true that only one in hundreds of millions of sperms ‘dare hope to survive’, the calculation looks very different from the point of view of a single gene. If we forget linkage groups and brand-new mutations for a moment, however rare a gene may be in the gene-pool, if a given male has it in his diploid genotype, at least 50 per cent of his sperms must have it. If one sperm has received a gene giving it competitive advantage, 50 per cent of its rivals in the same ejaculate will have received the same gene. Only if the mutation has arisen
de novo
during the genesis of a single sperm will the selection pressure be astronomical in magnitude. Usually it will be a more modest selection pressure, not of millions to one but only two to one. If we take linkage effects into consideration the calculation is more complicated, and the selection pressure in favour of competitive sperms will increase somewhat.

In any case, it is a strong enough pressure for us to expect that, if genes expressed themselves when in the haploid genotype of the sperm, outlaws would be favoured, to the detriment of the rest of the genes in the diploid father’s genome. It seems, to say the least, fortunate that sperm phenotypes are, as a matter of fact, usually not under the control of their own haploid genotypes (Beatty & Gluecksohn-Waelsch 1972). Of course sperm phenotypes must be under some genetic control, and natural selection has doubtless worked on the genes controlling sperm phenotypes to perfect sperm adaptation. But those genes seem to express themselves when in the diploid genotype of the father, not when in the haploid genotype of the sperm. When in the sperm they are passively carried.

The passivity of their genotypes may be an immediate consequence of the lack of cytoplasm in spermatozoa: a gene cannot achieve phenotypic
expression except via cytoplasm. This is a proximal explanation. But it is at least worth toying with reversing the proposition to obtain an ultimate functional explanation: sperms are made small, as an adaptation to prevent the phenotypic expression of the haploid genotype. On this hypothesis we are proposing an arms race between (haploid-expressed) genes for increased competitive ability among spermatozoa on the one hand, and genes expressing themselves when in the diploid genotype of the father on the other hand, causing sperms to become smaller and therefore unable to give phenotypic expression to their own haploid genotypes. This hypothesis does not explain why eggs are larger than sperms; it assumes the basic fact of anisogamy, and therefore does not aspire to be an alternative to theories of the origins of anisogamy (Parker 1978b; Maynard Smith 1978a; Alexander & Borgia 1979). Moreover not all sperms are small, as Sivinski (1980) reminds us in a most intriguing review. But the present explanation still deserves consideration as an ancillary to others. It is analogous to Hamilton’s (1967) explanation for the inertness of Y chromosomes, to which I have already alluded.

Some of the outlaws I have been considering have been realistic, and are actually known to geneticists. Some of the suggested outlaws that I shall now come to are, frankly, pretty improbable. I make no apology for this. I see them as thought experiments. They play the same role in helping me to think straight about reality as imaginary trains travelling at nearly the speed of light do for physicists.

So, in this spirit of thought experiment, imagine a gene on a Y chromosome which makes its possessor kill his daughters and feed them to his sons. This is clearly a behavioural version of a driving Y-chromosome effect. If it arose it would tend to spread for the same reason, and it would be an outlaw in the same sense that its phenotypic effect would be detrimental to the rest of the male’s genes. Modifiers, on any chromosome other than the Y chromosome, which tended to reduce the phenotypic effect of the daughter-killing gene would be favoured over their alleles. In a sense the outlaw gene is using the sex of the male’s children as a convenient
label
for the presence or absence of itself: all sons are labelled as definite possessors of the gene, all daughters as definite non-possessors of it.